June 10, 2014

What Happens Within A Fly’s Brain When Faced With An Incoming Predator?

The flight of a fruit fly, as determined by a recent study, is dependent upon whether or not the fly perceives a threat.

Scientists at the Howard Hughes Medical Institute's Janelia Research Campus have successfully discovered the brain processes engaged in standard flight and the more rapid escape flight. A quick-escape circuit in the fly's brain overrides the slower, more controlled behavior as a threat looms large over the insect.

“The fly's rapid takeoff is, on average, eight milliseconds faster than its more controlled takeoff,” said Janelia group leader Gwyneth Card. “Eight milliseconds could be the difference between life and death.” The quicker getaway appears to be somewhat clumsier than the more graceful slow takeoff.

According to Card, this study is meant to unravel the circuits and processes required for flash decision making in the fruit fly. What they learned is that there are two specific neural circuits responsible for mediating the slow-and-stable or quick-but-clumsy escape behaviors. When the neuron responsible for a quick takeoff receives a surge of activity, it effectively overrides the mechanisms at play for the slow escape. The result is that the fly, recognizing a threat, springs to safety.

Prior to this study, it was suspected that a pair of neurons – called giant fibers – were responsible for a fly's escape behaviors. Scientists were able to initiate this response via artificial activation of the giant fiber neurons. However, until this study, it was unknown whether or not those neurons actually responded to a visual cue of an impending attack from a predator.

In a device that is “really like a domed IMAX for the fly”, the researchers conducted their experiments on the fruit flies. Video, shooting at 6,000 frames per second, followed the fly as it was approached by a looming dark circle meant to mimic a potential predator, the damselfly. To perfect the approach of the darkened circle, Card teamed with Anthony Leonardo, also of the Janelia group, to record and analyze both the trajectories and accelerations of the damselfly as they attacked. “We wanted to make sure we were really challenging the animal with something that was like a predator attack,” Card explained.

The long and short escapes were discovered after careful analysis of more than 4,000 flies. In the long and steadier takeoff, a fly will take its time to raise their wings fully before committing to flight. Conversely, in an escape takeoff, this step was skipped. While the takeoff was milliseconds faster, it often resulted in a clumsy ascent that caused the fly to tumble through the air.

As noted above, researchers have been able to turn the response on and off in a fly's giant fiber neurons. What Card's team learned upon switching off the neurons was that flies were still able to complete the escape sequence. “On a surface level evaluation, silencing the neuron had absolutely no effect,” Card commented. “You can do away with this neuron that people thought was fundamental to this escape behavior, and flies still escape.” The escapes, however, were represented by the slower and more graceful takeoffs rather than the split-second flight responses.

It was only when the giant fiber neuron was switched back to the 'on' position that the emergency escape behaviors were observed again. The evidence suggests that the giant fiber neurons are only involved in the short escape behavior, while a separate circuit is responsible for the long escapes.

This finding led Card and her team to seek an understanding behind the decision making process for when a fly would sacrifice the stability of a long escape for the quicker response. Catherine von Reyn, a postdoctoral researcher in Card's lab, designed a set of experiments intended to monitor the activity within the giant fiber neurons. What she discovered confounded the team based on their findings to this point.

It became apparent the giant fiber neurons played an active role in both the short-mode and long-mode escapes. This added a layer of complexity to the results of their genetic experimentation they had not expected. “Seeing the dynamics of the electrophysiology allowed us to understand that the timing of the spike is important in determining the fly's choice of escape behavior,” Card noted.

After reviewing their collected data, Card and von Reyn believe the flight response, which initially yields to a slow escape, is initiated when a looming stimulus first activates a circuit in the brain. This begins the signature controlled lift of the wings. However, as the stimulative object grows ever closer, filling the fly's field of vision, the giant fiber activates. This activation leads to the clumsier but more urgent escape behavior.

“What determines whether a fly does a long-mode or short-mode escape is how soon after the wings go up the fly kicks its legs and it starts to take off,” Card explained. “The giant fiber can fire at any point during that sequence. It might not fire at all – in which case you get this nice long, beautifully choreographed takeoff.” She continued, “It might fire right away, in which case you get an abbreviated escape.”

This latest research is merely a continuation of Card's fascination with animal escape behaviors. She wants to continue research to determine how flies calculate the orientation of a threat and then decide in which direction to flee. She is also curious as to how a fly opts for a flight escape response over other evasive maneuvers. She claims the compact neural circuitry that controls sensory-driven behaviors provides a powerful system for exploring the mechanisms that animals use to select one behavior over another. “We think that you can really ask these questions at the level of individual neurons, and even individual spikes in those neurons,” she concluded.